The Neurology of Eye Movements, Edition 5, by R. John Leigh, M.D. and David S. Zee MD Foreword Chapter 1: A Survey of Eye Movements: Characteristics and Teleology Chapter 2: The Ocular Motor Periphery Chapter 3: The Vestibular-Optokinetic System Chapter 4: The Saccadic System Chapter 5: Smooth Visual Tracking and Fixation Chapter 6: Gaze Holding and The Neural Integrator Chapter 7: The Neural Basis for Conjugate Eye Movements Chapter 8: Eye-Head Movements Chapter 9: Vergence Eye Movements Chapter 10: Diagnosis of Peripheral Ocular Motor Palsies And Strabismus Chapter 11: Diagnosis of Nystagmus and Saccadic Intrusions Chapter 12: Diagnosis and Management of Vestibular Disorders Chapter 13: Disorders of Ocular Motility Due To Disease of the Brainstem, Cerebellum and Diencephalon Chapter 14: Disorders of Ocular Motility With Disease Affecting The Basal Ganglia, Cerebral Cortex, And In Systemic Conditions Appendix A: A Summary Scheme for the Bedside Ocular Motor Examination Appendix B: A Summary of Methods for Measuring Eye Movements Appendix C: Tables of Ocular Motor Findings in Hereditary Ataxias Appendix D: Table of Videos and their Legends

The neurology of eye movements

We recorded from single neurons in the middle temporal visual area (MT) of the macaque monkey and studied their direction and orientation selectivity. We also recorded from single striate cortex (V1) neurons in order to make direct comparisons with our observations in area MT. All animals were immobilized and anesthetized with nitrous oxide. Direction selectivity of 110 MT neurons was studied with three types of moving stimuli: slits, single spots, and random-dot fields. All of the MT neurons were found to be directionally selective using one or more of these stimuli. MT neurons exhibited a broad range of direction-tuning bandwidths to all stimuli (minimum = 32 degrees, maximum = 186 degrees, mean = 95 degrees). On average, responses were strongly unidirectional and of similar magnitude for all three stimulus types. Orientation selectivity of 89 MT neurons was studied with stationary flashed slits. Eighty-three percent were found to be orientation selective. Overall, orientation-tuning bandwidths were significantly narrower (mean = 64 degrees) than direction-tuning bandwidths for moving stimuli. Moreover, responses to stationary-oriented stimuli were generally smaller than those to moving stimuli. Direction selectivity of 55 V1 neurons was studied with moving slits; orientation selectivity of 52 V1 neurons was studied with stationary flashed slits. In V1, compared with MT, direction-tuning bandwidths were narrower (mean = 68 degrees). Moreover, V1 responses to moving stimuli were weaker, and bidirectional tuning was more common. The mean orientation-tuning bandwidth in V1 was also significantly narrower than that in MT (mean = 52 degrees), but the responses to stationary-oriented stimuli were of similar magnitude in the two areas. We examined the relationship between optimal direction and optimal orientation for MT neurons and found that 61% had an orientation preference nearly perpendicular to the preferred direction of motion, as is the case for all V1 neurons. However, another 29% of MT neurons had an orientation preference roughly parallel to the preferred direction. These observations, when considered together with recent reports claiming sensitivity of some MT neurons to moving visual patterns (39), suggest specific neural mechanisms underlying pattern-motion sensitivity in area MT. These results support the notion that area MT represents a further specialization over area V1 for stimulus motion processing. Furthermore, the marked similarities between direction and orientation tuning in area MT in macaque and owl monkey support the suggestion that these areas are homologues.

Direction and orientation selectivity of neurons in visual area MT of the macaque

The motor system may use internal predictive models of the motor apparatus to achieve better control than would be possible by negative feedback. Several theories have proposed that the cerebellum may form these predictive representations. In this article, we review these theories and try to unify them by reference to an engineering control model known as a Smith Predictor. We suggest that the cerebellum forms two types of internal model. One model is a forward predictive model of the motor apparatus (e.g., limb and muscle), providing a rapid prediction of the sensory consequences of each movement. The second model is of the time delays in the control loop (due to receptor and effector delays, axonal conductances, and cognitive processing delays). This model delays a copy of the rapid prediction so that it can be compared in temporal register with actual sensory feedback from the movement. The result of this comparison is used both to correct for errors in performance and as a training signal to learn the first model. We discuss evidence that the cerebellum could form both of these models and suggest that the cerebellum may hold at least two separate Smith Predictors. One, in the lateral cerebellum, would predict the movement outcome in visual, egocentric, or peripersonal coordinates. Another, in the intermediate cerebellum, would predict the consequences in motor coordinates. Generalization of the Smith Predictor theory is discussed in light of cerebellar involvement in nonmotor control systems, including autonomic functions and cognition.

Is the cerebellum a smith predictor

1. Eye movements were recorded in four rhesus monkeys, before and after bilateral ablations of the flocculi and portions of the paraflocculi (“flocculectomy”). Animals were trained to fixate and follow targets so that pursuit, saccades, and vestibular and optokinetic nystagmus could be quantitated. 2. The vestibuloocular reflex (VOR) was mildly affected by flocculectomy. In darkness the VOR gain (eye velocity/head velocity) for steps of head velocity (normal range, 0.84-0.96) increased postoperatively in one monkey to 1.17, decreased in another to 0.62, and did not change significantly in the other two (0.96, 0.94). VOR phase lead at 0.05-Hz oscillation in darkness (normal range, O,O--LOO) increased in two monkeys by 12 and 9.5 O but did not change significantly in the others. 3. Visual suppression of inappropriate vestibular nystagmus was impaired. During oscillation at 0.25 Hz with a head-fixed visual scene, the average amount of attenuation of the VOR decreased from 5 1% preoperatively to 20% postoperatively. Visual suppression of caloric nystagmus was comparably affected. 4. Smooth tracking of small targets moving in space was impaired either with the head still (smooth pursuit) or moving (cancellation of the VOR by fixating a target rotating with the head). The average gain (gaze velocity/target velocity) in either case was about 0.65 (normal, 0.95-0.98). The pursuit deficit was less than that reported after total cerebellectomy, suggesting other cerebellar structures also participate in smooth tracking. 5. Optokinetic nystagmus (OKN) was present postoperatively but, in response to a constant-velocity stimulus, the initial slowphase velocity decreased by 50% and the rise time to a steady state nearly doubled. For stimuli belowr 6O”/s the average steady-state gain was only mildly diminished to 0.86 (normal, 0.98) and the time course of optokinetic afternystagmus (OKAN) in darkness was normal. The response to higher velocity optokinetic stimuli was impaired. These abnormalities can largely be attributed to the coexisting pursuit deficit although the protracted rise to a steady state suggests a change in the ability of the brain stem optokinetic system to handle large amounts of retinal slip. 6. Flocculectomized monkeys showed horizontally, gaze-paretic nystagmus with exponentially decaying centripetal drift (time constant, 1.56 s) and vertically, downbeat nystagmus with exponentially decaying (in three monkeys) or exponentially increasing (in one monkey) slow phases. All animals showed rebound nystagmus. These results implicate the flocculus and possibly the paraflocculus in the control of the time constant and stability of the brain stem oculomotor integrators. 7. Saccadic velocities and accuracy were normal but flocculectomized monkeys showed brief (40150 ms duration), approximately exponential, postsaccadic drift with amplitudes up to 15% of the size of the saccade. The eyes usually drifted in the same direction as the saccade but each monkey showed an idiosyncratic pattern depending on saccade direction and eye position. Postsaccadic drift may reflect a mismatch between the phasic (pulse) and tonic (step) innervational changes that create saccades.

Effects of ablation of flocculus and paraflocculus of eye movements in primate

that area 7 of posterior parietal cortex plays a role in visual attention and eye movements. We have operationally defined attention as a stimulus-selection process independent of the specific movement used to respond to the stimulus. We trained monkeys to make various hand or eye movements and recorded from single neurons in area 7 while the monkeys were performing these tasks. 2. As demonstrated previously ( 19, 20, 46, 47, 63), many cells in area 7 respond to visual stimuli independent of any behavior. The discharge to a stimulus may be enhanced when the animal makes an eye movement to the stimulus. 3. We used two paradigms to study the modulation of visual responses when the animal used a stimulus without making an eye movement. The first was a peripheral-attention task in which the animal had to signal the occurrence of a peripheral stimulus without making an eye movement to it. Half of the cells studied gave an enhanced response in this task. In the second task, the animal had to reach out and touch a stimulus without making an eye movement to it. Visually responsive parietal neurons also yielded enhanced responses in this task. 4. The enhancements demonstrable in the saccade, peripheral-attention, and handreach tasks probably represent the same underlying process because their frequency of occurrence in our sample is almost identical, the intensities are quite similar, and cells that give an enhanced response on one task give an enhanced response in the others. 5. These results show that in posterior parietal cortex, the behavioral enhancement of a visual response is independent of the specific movement used to respond to the stimulus. The physiological mechanism of enhancement, which is movement independent and spatially selective, resembles the psychological phenomenon of selective spatial attention. We suggest that the role of area 7 in visual attention may be mediated by the enhancement of visual responses to selected stimuli.

Behavioral enhancement of visual responses in monkey cerebral cortex. I. Modulation in posterior parietal cortex related to selective visual attention

These experiments were designed to study the projections to the pons from visual and visual association cortex of monkeys by degeneration staining and horseradisch peroxidase (HRP) methods. When lesions were made in these cortical visual areas, degenerated fibers were found in the rostral dorsolateral area of the pontine nuclei. When HRP was injected among visually responsive cells in this region of the pons, layer V cortical pyramidal cells were labeled. These labeled cells were concentrated most heavily on both banks of the superior temporal and intraparietal fissures, and on the rostral bank of the parieto-occipital fissure. The efferent targets and receptive field properties of these cortical regions are consistent with their possible role in visual guidance of movement.

Corticopontine visual projections in macaque monkeys

Two hundred and thirty-two visually activated neurones were recorded in a small area of the rostral pontine nuclei of cats. The location of visually activated neurones was coextensive with the input from visual areas of cat's cortex as determined by degeneration studies. 2. Pontine visual cells could only be driven by visual stimuli. Cells responsive to somatosensory or auditory stimuli were also found in different regions in rostral pontine nuclei. They too responded to only one modality. 3. 96% of the cells were directionally selective. 4. Pontine visual cells were responsive to a wide range of stimulus speeds. Some cells responded to targets moving as fast as 1000 degrees/sec without losing directional selectivity. No pontine visual cells gave a clearly sustained response to a stationary stimulus. 5. Exact stimulus configurations were not critical. Large fields containing many spots were the most effective stimuli for 50% of the cells. Inhibition of responses depending upon stimulus dimensions, direction of movement, or location in the visual field was found for many cells. 6. Receptive field dimensions were large, ranging in size from 3 degrees X 4 degrees to more than an entire hemifield. 7. 94% of the cells had receptive fields which were centred in the contralateral hemifield. 8. 98% of the cells could be driven from both eyes. 9. The properties of the pontine visual cells suggest a corticopontocerebellar pathway sensitive to a wide range of speeds and directions of movement, but not sensitive to precise form.

https://physoc.onlinelibrary.wiley.com/doi/pdf/10.1113/jphysiol.1976.sp011287

Visual cells in the pontine nuclei of the cat.

1. The superior colliculus projects to the dorsolateral nucleus of the pons. Retrograde transport of horseradish peroxidase (HRP) revealed that cells in the superior colliculus, which send their ax...

Tectopontine pathway in the cat: laminar distribution of cells of origin and visual properties of target cells in dorsolateral pontine nucleus.

1. Area 18 projects to the rostral pontine nuclei. The visual response properties of rostral pontine cells differ greatly from those that have been reported for area 18 cells. We identified and studied corticopontine cells in area 18 and compared their receptive-field properties to those of other area 18 cells and to pontine visual cells. 2. We first located the visual area in the rostral pons by microelectrode recording and placed stimulating electrodes at the same site. Anti-dromically invaded cells were then recorded in area 18. The antidromic invasion of each cell was verified by orthodromic-antidromic spike collision. 3. Fifty-seven well-isolated corticopontine cells were studied in detail. We also recorded 466 unitary antidromic potentials with a mean invasion latency of 3.5 ms and recorded from 40 additional area 18 units to serve as a comparison group for the corticopontine cells. The comparison group cells were located in the same area in the visual field as the corticopontine cells. 4. The average receptive-field area for corticopontine cells (485 deg2) was much larger than the comparison cells (59 deg2). Forty percent of the corticopontine cells responded preferentially to multiple-spot target. Properly oriented gratings, slits, or edges were the most effective stimuli for the comparison cells. Eighty-two percent of the corticopontine cells showed clear directional preferences to moving-spot stimuli, and downward movements were most commonly preferred. Fifty-five percent of the area 18 comparison cells showed some directional preference, but no particular direction was preferred. The optimal stimulus speeds for corticopontine cells were higher than those for the comparison cells. 5. The response properties of the area 18 corticopontine cells are similar to the response properties of rostral pontine visual cells, except for a somewhat higher selectivity for orientation in the corticopontine cells. 6. We conclude that most response properties of rostral pontine visual cells are already present in a subset of area 18 cortical cells which project to the pons. The corticopontine cells are sensitive to multiple-spot targets moving in particular directions over large portions of the visual field, such properties are consistent with a visuomotor function for the corticopontocerebellar pathway.

Corticopontine cells in area 18 of the cat

1. Projections of pontine visual cells onto the cat cerebellar cortex were studied by antidromic activation and by the retrograde transport of horseradish peroxidase (HRP). 2. Cells in the medial pontine visual area, which receive visual cortex projections, were activated antidromically principally from the contralateral cerebellar hemisphere. Cells in the dorsolateral pontine visual area, which receive an input from the superior colliculus, were activated principally from the vermis and ipsilateral hemisphere. There is some overlap in the projections of these two different populations of pontine cells, which probably occurs by way of bifurcated axons. 3. The HRP technique confirmed that there is a major difference in the pattern of projections from these two pontine visual regions. Many cells in the rostral-medial portion of the pontine nuclei, which receive their input from visual cortex, were labeled following HRP injections in the contralateral cerebellar hemisphere. Far fewer of these cells were labeled following vermal injection. Cells in the dorsolateral pontine nucleus, which receive visual input from the superior colliculus, were labeled following an HRP injection in the vermis or the ipsilateral hemisphere. Cells in the region of pontine nuclei that receive input from the ventral lateral geniculate nucleus were also labeled after a vermian injection. 4. If the vermis is related to the control of whole-body movements and the hemisphere to control of ipsilateral limbs, these results suggest that the corticopontocerebellar and the tectopontocerebellar pathways may be involved in different classes of visually guided movement.

A. Gibson

Papers

Corticopontine visual projections in macaque monkeys

Visual cells in the pontine nuclei of the cat.

Tectopontine pathway in the cat: laminar distribution of cells of origin and visual properties of target cells in dorsolateral pontine nucleus.

Corticopontine cells in area 18 of the cat

Visual pontocerebellar projections in the cat